Interleukin-13 (IL-13)/IL-13 receptor alpha1 (IL-13Ralpha1) signaling regulates intestinal epithelial cystic fibrosis transmembrane conductance regulator channel-dependent Cl- secretion

J Biol Chem. 2011 Apr 15;286(15):13357-69. doi: 10.1074/jbc.M110.214965. Epub 2011 Feb 8.

Abstract

Interleukin-13 (IL-13) has been linked to the pathogenesis of inflammatory diseases of the gastrointestinal tract. It is postulated that IL-13 drives inflammatory lesions through the modulation of both hematopoietic and nonhematopoietic cell function in the intestine. To delineate the relevant contribution of elevated levels of intestinal IL-13 to intestinal structure and function, we generated an intestinal IL-13 transgenic mouse (iIL-13Tg). We show that constitutive overexpression of IL-13 in the small bowel induces modification of intestinal epithelial architecture (villus blunting, goblet cell hyperplasia, and increased epithelial proliferation) and epithelial function (altered basolateral → apical Cl(-) ion conductance). Pharmacological analyses in vitro and in vivo determined that elevated Cl(-) conductance is mediated by altered cystic fibrosis transmembrane conductance regulator expression and activity. Generation of iIL-13Tg/Il13rα1(-/-), iIL-13Tg/Il13rα2(-/-), and iIL-13Tg/Stat6(-/-) mice revealed that IL-13-mediated dysregulation of epithelial architecture and Cl(-) conductance is dependent on IL-13Rα1 and STAT-6. These observations demonstrate a central role for the IL-13/IL-13Rα1 pathway in the regulation of intestinal epithelial cell Cl(-) secretion via up-regulation of cystic fibrosis transmembrane conductance regulator, suggesting an important role for this pathway in secretory diarrhea.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Caco-2 Cells
  • Chlorides / metabolism*
  • Cystic Fibrosis Transmembrane Conductance Regulator / genetics
  • Cystic Fibrosis Transmembrane Conductance Regulator / metabolism*
  • Cysts / genetics
  • Cysts / metabolism
  • Cysts / pathology
  • Diarrhea / genetics
  • Diarrhea / metabolism
  • Diarrhea / pathology
  • Fibrosis
  • Humans
  • Interleukin-13 / genetics
  • Interleukin-13 / metabolism*
  • Interleukin-13 Receptor alpha1 Subunit / genetics
  • Interleukin-13 Receptor alpha1 Subunit / metabolism*
  • Intestinal Diseases / genetics
  • Intestinal Diseases / metabolism*
  • Intestinal Diseases / pathology
  • Intestinal Mucosa / metabolism*
  • Intestinal Mucosa / pathology
  • Ion Transport / genetics
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • STAT6 Transcription Factor / genetics
  • STAT6 Transcription Factor / metabolism

Substances

  • Chlorides
  • Il13ra1 protein, mouse
  • Interleukin-13
  • Interleukin-13 Receptor alpha1 Subunit
  • STAT6 Transcription Factor
  • Stat6 protein, mouse
  • Cystic Fibrosis Transmembrane Conductance Regulator